Long-term In-water Recaptures of Adult Black Turtles (Chelonia mydas) Provide Implications for Flipper Tagging Methods in the Eastern Pacific

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Herpetological Review 49(4), 2018
ARTICLES 653
Herpetological Review, 2018, 49(4), 653–657.
© 2018 by Society for the Study of Amphibians and Reptiles
Long-term In-water Recaptures of Adult Black Turtles
(Chelonia mydas) Provide Implications for Flipper
Tagging Methods in the Eastern Pacic
Black Turtles, also known as Eastern Pacific Green Turtles
(Chelonia mydas), are generally confined to the Eastern Pacific.
This population is composed of three major nesting rookeries
located in Colola, México, the Galápagos Islands, Ecuador and
Costa Rica (Seminoff et al. 2015). At the largest rookery at Co-
lola Beach, Mexico, more than 18,000 adult females have been
flipper tagged since 1983 (Delgado-Trejo 2002). Flipper tag re-
turns, satellite tracking data and genetic studies show that Black
Turtles 2from Colola Beach are found from San Diego Bay (USA)
to Central and South America (Alvarado and Figueroa 1992; By-
les et al. 1995; Lemons et al. 2011; Hart et al. 2015; Chaves et al.
2017).
As with other sea turtle populations, Black Turtles undertake
long-distance migrations during their life cycles (Bolten 2003)
and aggregate at foraging grounds, which are commonly shared
by individuals from different natal origins (Amorocho et al. 2012).
Connecting these foraging grounds to their reproductive sites is
vital for the implementation of effective regional conservation
strategies for this endangered species (IUCN 2018). Furthermore,
long-term studies using capture-mark-recapture methods have
provided information on population size, residency, site fidelity
and growth, as well as survival and recruitment rates, which are
vital components in sea turtle population assessments (see for
example Meylan et al. 2011; Pfaller et al. 2018). The most widely
used tool is the application of uniquely numbered external flip-
per tags, as they are easy to apply and sufficiently economical for
most monitoring programs to acquire. However, to be effective,
this method requires the direct recapture of tagged turtles and
broad networking by researchers.
MAIKE HEIDEMEYER*
Centro de Investigación en Biología Celular y Molecular (CIBCM),
Centro de Investigación en Ciencias del Mar y Limnología (CIMAR),
Universidad de Costa Rica, Ciudad de Investigación,
11501-2060, San Pedro, San José, Costa Rica
CARLOS DELGADO-TREJO
Instituto de Investigaciones sobre los Recursos Naturales
Departamento de Ecología Marina, Universidad Michoacana de
San Nicolás de Hidalgo, Av. San Juanito Itzícuaro s/n,58004 Morelia,
Michoacán de Ocampo, Mexico
CATHERINE E. HART
Grupo Tortuguero de las Californias, A.C. Calle 6, Las Azaleas,
23090 La Paz, Baja California Sur, Mexico
Investigación, Capacitación y Soluciones Ambientales y S ociales A.C. (ICSAS),
Acaponeta #358, Col. Morelos 63160, Tepic, Nayarit, Mexico
CHELSEA CLYDE-BROCKWAY
Department of Forestry and Natural Resources, Purdue University,
715 W State St, West Lafayette, Indiana 47907, USA
LUIS G. FO NSECA
Latin American Sea Turtles (LAST), 496-1100 Tibás,
San José, Costa Rica
RANDALL MORA
MARLON MORA
ANIBAL LARA
RICARDO OBANDO
Asociación para la Conservación Integral de Recursos Naturales
Equipo Tora Carey (ETC), 500m E of the Police Station, El Jobo,
51001 La Cruz, Guanacaste, Costa Rica
Corresponding author; e-mail: maike.heidemeyer@gmail.com
aPPendix 5
Correlations between univariate characters and principal components
(PCs) and between PCs included in the canonical variate analysis
model and canonical variate 1 (CV1) derived from a CVA of Classes
A and B of Aspidoscelis sonorae from Cave Creek Canyon, Chiricahua
Mtns., Cochise County, Arizona.
Variables PC1 PC3 PC4 CV1
FP 0.468 -0.488 0.015
GAB 0.825 -0.191 -0.012
SPV 0.378 0.043 0.440
COS 0.476 0.450 0.439
LSG 0.838 -0.127 -0.038
SDL-T4 0.477 0.324 -0.719
SDL-F4 0.138 0.780 0.021
PC1 -0.453
PC3 -0.407
PC4 0.231
Eigenvalues 2.218 1.208 0.906 2.274
Percentage of variation summarized 31.7 17.3 12.9 100

Herpetological Review 49(4), 2018
654 ARTICLES
The success of flipper tagging programs is influenced by
tag loss (when an individual loses a portion or all of its initial
marking), which varies between tag type, studied species, and
where the tag is attached to the turtle (Green 1979; Limpus 1992;
Strong e t al. 19 93, Pfaller et al. 2018). Furthermore, th e recapture
rate (proportion of tagged individuals recovered of all individuals
tagged) of flipper tagged sea turtles between nesting beaches and
foraging grounds is generally low, especially in Black Turtles as few
in-water monitoring projects exist within the Black Turtles’ range.
In recent years, sampling effort at foraging grounds has increased,
and, theoretically, with it the likelihood of recovering females
previously tagged at their nesting beaches, where monitoring
programs are well established. However, so far, there are only
three reports of recaptures nesting females at ongoing in-water
monitoring projects in the Eastern Pacific, all of which occurred
within three years after initial tagging at their nesting beach: two
originating from the Galapagos Archipelago, one of which was
recaptured in Golfo Dulce, South Pacific of Costa Rica (Chacón-
Chaverrí et al. 2015) and the other at El Ñuro in Peru (Velez-Zuazo
et al. 2014), and one originating at the Colola rookery, which was
recaptured in the Gulf of California (Seminoff et al. 2002).
One of the few in-water projects along the Pacific coast of
Costa Rica is located in Matapalito Bay, which was monitored
sporadically starting in 2012, before regular monthly surveys
were established in 2016. Matapalito Bay hosts a foraging
ground for different Black Turtle and yellow-morph Green
Turtle populations, as well as Hawksbill Turtles (Eretmochelys
imbricata) (Heidemeyer et al. 2014). Here, we present the first
recapture of an adult female originating from the Colola nesting
rookery at the Matapalito foraging ground after 16 years since
initial tagging. This is the longest recapture period registered
in the Eastern Pacific, which we attribute to differential tag
retention rates obtained from adult Black Turtles recaptured at
Matapalito Bay. To put the importance of both tagging methods
and regionally increased coverage of foraging ground surveys
into context, we discuss tag retention rates reported to date and
present previously unanalyzed data from adult females tagged
and recaptured at Colola Beach between the years 1981–2000
(Figueroa et al. 1993; Delgado-Trejo 2002).
Methods
In Matapalito Bay (10.93382°N, 85.79378°W; WGS 84), we
captured foraging sea turtles using three specially designed tur-
tle entanglement nets made of black silk twine measuring 240
m in length, 8 m in depth and 42 cm in mesh size, set in series
with each other. Sampling took place one to two times a month
year-round (weather permitting); during each sampling day,
nets were set in the morning adjacent to the reef with care to
avoid damaging the reef, checked every 20–40 min, and removed
after 3–4 h (see Heidemeyer et al. 2014). Upon capture, turtles
were brought onto the research boat where a standard protocol
was followed (Heidemeyer et al. 2014), which included measur-
ing curved carapace length (CCL) and curved carapace width
(CCW), weight, and tissue sampling. Turtles were occasionally
tagged with internal passive integrated transponder (PIT) tags
(AVID). Prior to September 2017, all turtles were double tagged
through the second scale of each of their front flippers with In-
conel tags (Style 681IC, National Band and Tag Company). How-
ever, in September 2017, the tagging procedure was modified to
apply flipper tags only to the skin adjacent to the first inner scale
of both hind flippers (Fig. 1A).
On Colola Beach (18.29536°N, 103.41172°W ), nightly patrols
were carried out from September to December between 1981–
2000. Turtles were intercepted when they came out of the ocean
to nest and data was collected for a long-term database on adult
health and reproductive output (Figueroa et al. 1993; Delgado-
Trejo 2002). Approximately 2–5% of all females encountered
were measured with a flexible measuring tape (0.5 cm precision,
same methods used at Matapalito Bay) to take curved carapace
lengths (CCL) and tagged with one uniquely numbered Inconel
metal tag applied through the skin adjacent to the first inner
scale of the left hind flipper (Fig. 1A). For all recaptured indi-
viduals, we calculated flipper specific tag retention by counting
the number of tags retained upon the turtle’s recapture and es-
timated recapture periods defined in days at large from the day
the turtle was initially tagged until the day it was last recaptured.
Fig. 1. A) Location of hind flipper tag. B) condition of recaptured female Black Turtle hind flipper and Inconel tag after 5832 days.

Herpetological Review 49(4), 2018
ARTICLES 655
results
On 8 December 2017, we captured an adult female Black
Turtle with left hind flipper tag HA862 in Matapalito Bay, Costa
Rica. The tag showed little impact of encrusting organisms or al-
gae coverage (Fig. 1B). We quickly obtained the turtle’s nesting
beach origin via a request for information to the Latin American
sea turtle research group. The nesting female was initially tagged
on Colola Beach, Michoacán, Mexico, on 21 September 2001, af-
ter successfully depositing a clutch of 81 eggs at which time she
measured 86.0 cm CCL. Upon the turtle’s recapture 5832 days
(about 16 years) later, she measured 87.0 cm CCL. This turtle rep-
resents the longest recapture period of all tag recoveries both at
nesting beaches and foraging grounds for individuals originally
tagged at Colola Beach, and to best of our knowledge, for the en-
tire Eastern Pacific.
Additionally, we tagged and recaptured two male Black Tur-
tles in Matapalito Bay, after 319 and 1622 days, respectively. Both
turtles had lost at least one of their front flipper tags (Table 1).
Turtle ID SE-A-25 had lost his right front flipper tag and turtle ID
SE-A-5 had lost both of its front flipper tags and was identified by
its internal PIT tag. Turtle ID SE-A-Cm-25 increased in size be-
tween initial capture and recapture, but the other turtle did not.
discussion
Hind flippers are the position of choice for applying flipper
tags to sub-adult and adult Black Turtles, as evidenced here of the
longest recapture period in the Eastern Pacific of a flipper tagged
female turtle from the Colola nesting rookery after 16 years. In
Colola, most nesting females are tagged with only one Inconel
metal tag in their left hind flipper, where tags have a greater re-
tention probability when compared to front flippers (Strong et al.
1993) and have previously proven to stay intact over several years
(Senko et al. 2010). Tag retention has been identified as an under-
lying factor in assessing sea turtle populations and age-specific
survival rates (Pfaller et al. 2018), which is why different moni-
toring projects covering a population’s biogeography should use
standardized tagging methods with the longest retention rates.
An initial study comparing tag type and position at Colola
conducted by Alvarado et al. (1988) found that monel metal tags
applied in front flippers were lost by more than 44% compared
to plastic tags in hind flippers, where tag loss was about 2.8%.
Similar results were found by Green (1979). These authors
attributed tag loss to the type of tag rather than tag position.
Similarly, Green (1984) and Alvarado-Díaz and Figueroa
(1992) mention the application of both metal and plastic tags,
respectively, on front and hind flippers, yet it is unclear which tag
position proved most effective in their long-distance tag recovery
studies. Following this uncertainty, Strong et al. (1993) compared
the retention of metal tags on all four flippers of nesting females
and found that tags applied to the left hind flipper are retained
longest, although differences were not significant, possibly due
to small sample size and short sampling period (one nesting
season). Nonetheless, the tagging of hind flippers was suggested
in a handbook on Research and Management Techniques for
the Conservation of Sea Turtles (Balazs 1999), particularly for
tagging adult turtles on nesting beaches.
In the Eastern Pacific however, most Black Turtle monitoring
projects, including the major nesting beaches at the Galapagos
Islands and Costa Rica apply metal (Inconel) tags on their front
flippers, either on or close to the trailing edge (Zárate and Dut-
ton 2002; Santidrián-Tomillo et al. 2014), and this position and
tag type is also used at the majority of the currently operating
projects at Black Turtle foraging grounds (Amorocho et al. 2007;
Heidemeyer et al. 2014; Velez-Zuazo et al. 2014, Chacón-Chaver-
ri et al. 2015; Zárate et al. 2015; Álvarez-Varas et al. 2017; Karam-
Martínez et al. 2017). In other Green Turtle populations, front
flipper tags have proven viable over time, where tag recaptures
are reported after 12 yrs in Australia (Limpus and Chaloupka
1997) and up to 29 yrs in Hawaii (Nurzia-Humburg and Balazs
2014). Furthermore, Limpus (1992) showed that in Australia,
hind flipper metal tags were lost at a higher rate than tags of the
same type placed in front flippers and that tag loss was greater in
turtles tagged on nesting beaches than those tagged at foraging
grounds. To the best of our knowledge, the only foraging ground
study that has quantified tag loss in the Eastern Pacific was con-
ducted in Golfo Dulce, in South Pacific Costa Rica, where 60% of
all recaptured Black Turtles had lost at least one tag in less than
730 days (Chacón-Chaverri et al. 2015). This elevated tag loss in
front flipper tagged turtles is also reflected in the two male Black
Turtles tagged and recaptured in Matapalito Bay, which lost one
and both of their tags after 319 and 1622 days, respectively. At
least in adult turtles, the apparent higher tag loss from front flip-
pers might be a result of the aggressive mating behavior exhib-
ited by male turtles, which could result in the removal of flipper
tags during courtship (Balazs 1982; Limpus 1992). The relatively
rapid loss of the front flipper tags in the two male Black Turtles
reported herein thus might suggest that they were reproductive-
ly active since their first capture.
It is unknown why most monito ring proje cts prefer the deploy-
ment of tags on Black Turtles’ front flippers, as there is no pub-
lished information available that recommends this method over
hind flipper tagging in the Eastern Pacific. On the contrary, the
little information available on tag retention periods in the Eastern
Pacific suggests that hind flipper tags are more effective for adult
table 1. Morphometric data and tag retention rate of three adult Black Turtles (Chelonia mydas) recaptured in Matapalito Bay after initial tag-
ging at either foraging ground (FG) or nesting ground (NG) with tags applied in different flippers and positions (L = left, R = right). Dashed line
indicates no tag originally placed in that location.
First capture Recapture Tag retention
Turtle ID Sex Location CCL Location CCL L front R front L hind Overall tag Days
(cm) (cm) flipper flipper flipper retention at large
scale scale skin (%)
SE-A-Cm-25 M Matapalito Bay (FG) 82.5 Matapalito Bay (FG) 84 1 0 – 50 319
SE-A-Cm-5 M Matapalito Bay (FG) 77 Matapalito Bay (FG) 77 0 0 – 0 1622
HA862 F Colola Beach (NG) 86 Matapalito Bay (FG) 87 – – 1 100 5832

Herpetological Review 49(4), 2018
656 ARTICLES
Black Turtles at nesting beaches (Strong et al. 1992; this study), as
well as for juvenile Black Turtles at foraging ground habitats. For
instance, Senko et al. (2010) tagged and recaptured two juvenile
Black Turtles at foraging grounds in Baja California Sur with both
of their hind flipper tags present after 183 and 2038 days. Baja Cali-
fornia in Mexico (López-Castro et al. 2010, Senko et al. 2010), Pá-
racas in Peru (Velez-Zuazo et al. 2014) and now Matapalito Bay are
the only foraging ground sites to our knowledge where hind flip-
per tags are applied. Unfortunately, the vast majority of published
sea turtle foraging ground studies do not include any information
on tag loss or retention when reporting on recaptured individu-
als. This hinders proper estimations of the underlying factors that
might be associated to the probability of tag recoveries, such as
turtle size and age, behavior, habitat use and ocean basin, as well
as researchers’ experience in applying tags and monitoring efforts.
Most published studies on tag retentions are currently retrieved
from adult females showing nesting site fidelity (Bjorndal et al.
1996; Pfaller et al. 2018), which results in higher tag recovery rates
and represents a more realistic estimate of tag retention probabili-
ties than those at foraging grounds due to intensive beach moni-
toring throughout the nesting season. Thus, to fully understand
the apparent higher tag loss in front flippers, longer retention
rates in hind flippers and the importance of tag loss in the overall
low tag recovery, tag retention rates at both nesting grounds and
foraging sites in the Eastern Pacific and across all available life
stages need to be further investigated.
Aside from tag loss, another reason for the overall low recap-
ture rates of Black Turtles tagged at their nesting grounds, is the
likelihood that both developmental and foraging grounds of Black
Tur t le s a re n ot ye t s u ff ic i en tl y id en t if ie d a n d s tu d ie d. Tod ay, st i ll
the large majority of reported tag returns from nesting rookeries
within the Eastern Pacific originate from fisheries-dependent re-
captures, particularly along the Central American coast (Green
1979; Alvarado-Díaz and Figueroa 1992). For instance, of the more
than 18,000 Black Turtles tagged at Colola Beach, 71 recaptured
females were reported by fishermen in incidental captures (Al-
varado-Díaz and Figueroa 1992) and only two at ongoing in-wa-
ter monitoring efforts of Black Turtle foraging grounds (Seminoff
et al. 2002; this study, Fig. 2). Because the circumstances (i.e., pre-
cise location of recapture) of fisheries-dependent recaptured sea
turtles are often uncertain (Green 1979; Cornelius and Robinson
1986; Alvarado-Díaz and Figueroa 1992), any conclusions on mi-
gration routes from these reports should be treated with caution.
Nonetheless, incidental recaptures as reported by Alvarado-Díaz
and Figuerora (1992) provided first evidence for the migration of
adult Black Turtles nesting at Colola Beach to Costa Rica, with our
finding of an adult female recaptured at the Matapalito Bay forag-
ing ground supporting this early report.
There has been a notable decrease of available information
on tag returns for turtles tagged at Colola Beach since 1990, when
Mexico imp osed a total nationwide ban on the capture, slaughter,
and consumption of sea turtles and their byproducts (Alvarado-
Díaz and Figueroa 1990; 1992). Once the ban was implemented,
reports by fishers and fisheries vessels reduced significantly, like-
ly due to the fear of possible sanctions (Cornelius and Robinson
1985; Alvarado-Díaz and Figueroa 1992). However, several sea
turtle networks have been established in the region since 1990,
and this should have resulted in an increase in tag returns. The
absence of these may indicate a lack of communication between
research groups or simply the need for greater monitoring effort
at foraging grounds, specifically those used by females nesting
at Colola Beach. Therefore, we recommend an extensive region
wide revision of flipper tagging and recapture databases, which
could hold further data on Black Turtle movements.
In conclusion, the best available data in the Eastern Pacific
suggest that changes in the location of tag placement in Black
Turtles from front to hind flippers may increase the probability
for tag returns allowing for more effective long-term monitoring
of Black Turtle populations. Nonetheless, a comparative study
of flipper tag positions and respective retention rates should be
conducted in the near future at both nesting beaches and for-
aging grounds in the Eastern Pacific to account for statistically
valid results. Furthermore, we encourage other researchers in
the Eastern Pacific to publish data concerning tag recoveries,
and that studies on recaptured animals include tag retentions as
well. Tag retention over time will allow us to answer questions
about the fidelity of Black Turtles in Matapalito Bay foraging site
and lay the ground work for the movement of tag placement in
other species that may be suffering from the same level of tag
loss and/or understudied habitats. We continue to monitor the
populations of turtles found in Matapalito Bay with repeated
sampling and hope to be able to achieve saturation tagging and
therein accomplish a long-term study that allows for more sub-
stantial estimates on the importance of tag loss and recovery
when assessing population parameters.
Acknowledgements.—We thank The Leatherback Trust, Red In-
tegral para el Estudio de Tortugas Marinas (RITMA) and the Vice-
Rectory for Research of the University of Costa Rica for financial
support. We are grateful for the field assistance of the numerous vol-
unteers and collaborators of Equipo Tora Carey, including Mathilde
Giry, as well as Sebastian Hernández and his students of the Centro
de Programas Internacionales (CPI) of Veritas University and Seeds
of Change. We thank the Guanacaste Conservation Area (ACG) of the
Sistema Nacional de Áreas de Conservación (SINAC) for research
permits in Matapalito Bay (ACG-PI-050-2014, ACG-PI-057-2016),
and particularly Roger Blanco and María Marta Chavarría. We thank
Javier Alvarado Díaz, Cutzi Bedolla Ochoa from Universidad Michoa-
cana de San Nicolas de Hidalgo and Hector Díaz Orcino from Grupo
Tortuguero de Colola, in Michoacán, Mexico, for assistance in the
collection of field data and the U.S. Fish and Wildlife Fund for pro-
viding funding for the Colola Beach monitoring project.
Fig. 2. Recapture periods of female Black Turtles (Chelonia mydas)
tagged at Colola Beach and recaptured at their nesting beach (white
bars), in fisheries incidences (gray bars) and at monitored foraging
grounds (black bars). Data obtained from Figueroa et al. (1993), Del-
gado-Trejo (2002), and Seminoff et al. (2002). Asterisk (*) indicates
the female (ID: HA862) recaptured in this study.

Herpetological Review 49(4), 2018
ARTICLES 657
literature cited
aMorocho, d. F., and r. d. reina. 2007. Feeding ecology of the East
Pacific green sea turtle Chelonia mydas agassizii at Gorgona Na-
tional. Endang. Spec. Res. 3:43–51.
———, F. a. abreu-grobois, P. h. dutton, and r. d. reina. 2012. Mul-
tiple distant origins for green sea turtles aggregating off Gorgona
Island in the Colombian Eastern Pacific. PLoS ONE 7:e31486.
alvarado-díaz, J., and a. Figueroa. 1990. Ecological Recovery of Black
Sea Turtle populations in Michoacan. Final Report for USFWS and
WWF-US.
———, and ———. 1992. Recapturas post-anidatorias de hembras de
tortuga marina negra Chelonia agassizii marcadas en Michoacán,
Mexico. Biotropica 24:560–566.
———, ———, and P. alarcon. 1988. Black turtle project in Micho-
acan, Mexico: Plastic vs. metal tags. Mar. Turt. Newsl. 42: 5–6.
áLvarez-varaS, r., J. Contardo, M. heideMeyer, L. Forero-rozo, b. bri-
to, v. cortes, M. J. brain, s. Pereira, and J. a. vianna. 2017. Ecology,
health and genetic characterization of the southernmost green
turtle (Chelonia mydas) aggregation in the Eastern Pacific: impli-
cations for local conservation strategies. Lat. Am. J. Aquat. Res.
45:540–554.
balazs, g. h. 1982. Factors affecting the retention of metal tags on sea
turtles. Mar. Turt. Newsl. 20:11–14.
———. 1999. Factors to consider in the tagging of sea turtles. In K.
L. Eckert, K. A. Bjorndal, F. A. Abreu-Grobois, and M. Donnelly
(eds.), Research and Management Techniques for the Conserva-
tion of Sea Turtles, pp. 101–109. IUCN/SSC Marine Turtle Special-
ist Group Publication No. 4. Washington, D.C. http://www.iucn-
mtsg.org/publications/Tech_Manual/17- balazs.pdf.
bJorndal, k. a., a. b. bolten, c. J. lagueux, and a. chaves. 1996. Prob-
ability of tag loss in green turtles nesting at Tortuguero, Costa Rica.
J. Herpetol. 30:567–571.
bolten, a. b. 2003. Variation in sea turtle life history patterns: Neritic
vs. oceanic developmental stages. In P. L. Lutz, J. A. Musick, and
J. Wyneken (eds.), The Biology of Sea Turtles, Vol. II, pp. 243–257.
CRC Press, Boca Raton, Florida.
byles, r., J. alvarado, and d. rostal. 1995. Preliminary analysis of
post-nesting movements of the Black Turtle (Chelonia agassizi)
from Michoacán, México. In J. I. Richardson and T. H. Richardson
(comps.), Proceedings of the 12th Annual Workshop on Sea Turtle
Biology and Conservation, pp. 12–13. NOAA Tech. Memo. NMFS-
SEFSC-361.
chacón-chaverri, d., d. a. Martínez-cascante, d. roJas, and l. g. Fonse-
ca. 2015. Captura por unidad de esfuerzo y estructura poblacional
de la tortuga verde de Pacífico (Chelonia mydas) en el Golfo Dulce,
Costa Rica. Int. J. Trop. Biol. 63:363–373.
chaves, J. a., M. Peña, J. a. valdés-uribe, J. P. Muñoz-Pérez, F. valleJo,
M. heideMeyer, and o. torres-carvaJal. 2017. Connectivity, popula-
tion structure, and conservation of Ecuadorian green sea turtles.
Endanger. Species Res. 32:251–264.
cornelius, s. e., and d. c. robinson. 1986. Post-nesting movements of
female olive ridley turtles tagged in Costa Rica. Vida Silvestre Neo-
tropical 1:12–23.
delgado-treJo, c. 2002. Historia de Vida y Conservación de la Po-
blación de Tortuga Negra (Chelonia agassizii) que anida en Mi-
choacán. Master’s Thesis, Universidad Michoacana de San Nicolás
de Hidalgo, Morelia, Michoacan, Mexico. 109 pp.
FiGueroa, a., J. aLvarado-díaz, F. hernández, G. rodríGuez, J. robLeS, and
J. alvarado. 1993. Population recovery of the sea turtles of Micho-
acán, Mexico: an integrated conservation approach. 1991–1992.
Final Report for USFWS and WWF-US.
green, d. 1979. Double tagging of green turtles in the Galapagos Is-
lands. Mar. Turt. Newsl. 4–9.
———. 1984. Long-distance movements of Galapagos green turtles.
J. Herpetol. 18:121–130.
hart, c. e., g. s. blanco, M. s. coyne, c. delgado-treJo, b. J. godley,
t. t. Jones, a. resendiz, J. a. seMinoFF, J. W. Witt, and W. J. nichols.
2015. Multinational tagging efforts illustrate regional scale of dis-
tribution and threats for East Pacific green turtles (Chelonia mydas
agassizii). PLoS ONE 10:e0116225.
heideMeyer, M., r. arauz-vargas, and e. lóPez-agüero. 2014. New for-
aging grounds for hawksbill (Eretmochelys imbricata) and green
turtles (Chelonia mydas) along the northern Pacific coast of Costa
Rica, Central America. Int. J. Trop. Biol. 62:109–118.
iucn. 2017. The IUCN Red List of Threatened Species. Version 2017–
1. http://www.iucnredlist.org. Downloaded on 05 December 2017.
karaM-Martínez, S. G., i. rayMundo-GonzáLez, J. a. Montoya-Márquez, F.
villegas-zurita, and F. becerril-bobadilla. 2017. Characterization of
a green turtle (Chelonia mydas) foraging aggregation along the pa-
cific coast of southern Mexico. Herpetol. Conserv. Biol. 12:477–487.
leMons, g. e., r. l. leWison, l. M. koMoroske, a. r. gaos, c.-t. lai, P.
h. dutton, t. eguchi, r. a. leroux, and J. a. seMinoFF. 2011. Trophic
ecology of green sea turtles in a highly urbanized bay: Insights
from stable isotopes and mixing models. J. Exp. Mar. Bio. Ecol.
405:25–32.
liMPus, c. J. 1992. Estimation of tag loss in marine turtle research.
Wildl. Res. 19:457–469.
———, and M. y. chalouPka. 1997. Nonparametric regression model-
ling of green sea turtle growth rates (southern Great Barrier Reef).
Mar. Ecol. Prog. Ser. 146:1–8.
lóPez-castro, M. c., v. koch, a. Mariscal-loza, and W. J. nichols. 2010.
Long-term monitoring of black turtles Chelonia mydas at coastal
foraging areas off the Baja California Peninsula. Endang. Spe-
cies Res. 11:35–45.
Meylan, P. a., a. b. Meylan, and J. a. gray. 2011. The ecology and migra-
tions of sea turtles 8. Tests of the developmental habitat hypoth-
esis. Bull. Am. Mus. Nat. Hist. 357:1–77.
nurzia-huMburg, i. n., and g. h. balazs. 2014. Forty years of research:
recovery records of green turtles observed or originally tagged
at French Frigate Shoals in the northwestern Hawaiian Islands,
1973–2013, NOAA Tech. Memo. NMFS-PIFSC-40. 20 pp.
PFaller, J. b., M. chalouPka, a. b. bolten, and k. a. bJorndal. 2018. Phy-
logeny, biogeography and methodology: a meta-analytic perspec-
tive on heterogeneity in adult marine turtle survival rates. Sci. Rep.
8:5852.
Santidrián-toMiLLo, P., S. a. robertS, r. hernández, J. r. SPotiLa, and F.
v. Paladino. 2014. Nesting ecology of East Pacific green turtles at
Playa Cabuyal, Gulf of Papagayo, Costa Rica. Mar. Ecol. 36:1–11.
seMinoFF, J. a., J. alvarado, c. delgado, J. l. loPez, and g. hoeFFer. 2002.
First direct evidence of migration by an East Pacific green seatur-
tle from Michoacan, Mexico to a feeding ground on the Sonoran
coast of the Gulf of California. Southwest. Nat. 47:314–316.
––––––, C. d. aLLen, G. h. balazs, P. h. dutton, t. eguchi, h. l. haas, s.
a. hargrove, M. P. Jensen, d. l. kleMM, a. M. lauritsen, s. l. MacPher-
son, P. oPay, e. e. Possardt, s. Pultz, e. seney, k. s. van houtan, and
r. s. WaPles. 2015. Status Review of the Green Turtle (Chelonia
mydas) under the Endangered Species Act. NOAA Tech. Memo.,
NOAA- NMFS-SWFSC–539. 571 pp. https://repository.library.
noaa.gov/view/noaa/4922
senko, J., M. c. lóPez-castro, v. koch, and W. J. nichols. 2010. Imma-
ture East Pacific green turtles (Chelonia mydas) use multiple for-
aging areas off the Pacific Coast of Baja California Sur, Mexico: first
evidence from mark-recapture data. Pacific Sci., 64:125–130.
strong, d., b. leatherMan, and b. h. brattstroM. 1993. Differential re-
tention of metal and plastic tags on the black sea turtle (Chelonia
agassizi). Herpetol. Rev. 24:23–24.
velez-zuazo, x., J. Quiñones, a. s. Pacheco, l. klinge, e. Paredes, s.
QuisPe, and s. kelez. 2014. Fast growing, healthy and resident green
turtles (Chelonia mydas) at two neritic sites in the central and
northern coast of Peru: Implications for conservation. PLoS ONE
9: e113068.
zarate, P., and P. dutton. 2002. Tortuga verde. In E. Danulat and G.
J. Edgar (eds.), Reserva Marina de Galápagos. Línea base de la
Biodiversidad, pp. 305–323. Fundación Charles Darwin/Servicio
Parque Nacional Galápagos, Santa Cruz, Galápagos, Ecuador.

ISSN 0018-084X Herpetological
Review
Herpetological
Review
VOLUME 49, NUMBER 4
DECEMBER 2018
The Ocial Bulletin of the
SOCIETY FOR THE STUDY OF AMPHIBIANS AND REPTILES
ARTICLES
The Louisiana Pinesnake (Pituophis ruthveni): At Risk of Extinction?
D. C. RUDOLP H, J. B. PIERCE, N. E. KO ERTH ................................................... 609
Rediscovery of the Booroolong Frog, Litoria booroolongensis, on the
Australian New England Tablelands after More than 40 Years
J. J. L. ROWL EY, T. P. CU TA JAR ....................................................................... 620
Automated Monitoring Techniques Reveal New Proximate Cues of
Houston Toad Chorusing Behavior
A. R. MACLAREN, S. F. MCCRACKEN, M. R. J. FORSTNER .................................. 622
The Function of Supplementary Notes in the Communication System
of Johnstone’s Whistling Frog, Eleutherodactylus johnstonei
S. V. FLECHAS, J. E. ORTEGA-CHINCHI LLA, L. M. ARENA S,
A. AMÉZQU ITA ............................................................................................626
Diversity of Anurans in Rice Fields under Organic and Conventional
Management in Santa Fe Province, Argentina
A. M. ATTADEMO, R. E. LORE NZÓN, P. M. PELTZER, R. C. LAJMANOVICH ........ 632
Relegation of Aspidoscelis flagellicaudus to the Synonymy of the
Parthenogenetic Teiid Lizard A. sonorae Based on Morphological
Evidence and a Review of Relevant Genetic Data
H. L. TAYLOR, C. J. COLE, C. R. TOWNSEND .................................................... 636
Long-term In-water Recaptures of Adult Black Turtles (Chelonia mydas)
Provide Implications for Flipper Tagging Methods in the Eastern Pacific
M. HEIDEMEYER, C. DELGADO-TREJO, C. E. HART, C. CLYDE-BROCKWAY,
L. G. FONS ECA, R. MORA, M. MORA, A. L ARA, R. OBANDO ............................ 653
Advertisement Call of the Glass Frogs Centrolene bacatum and
Centrolene buckleyi (Anura: Centrolenidae) from the Napo Region
of Ecuador
K. L. OTTO, P. M. HAMPTON .......................................................................... 658
TECHNIQUES
Use of a Non-Invasive Technique to Identify Individual Cave
Salamanders, Eurycea lucifuga
J. G. BRAD LEY, P. K. EASON ........................................................................... 660
A Portable, Low-cost Approach for Photographing Fluid-Preserved
Snake Specimens: Recommendations with Comments on Optimizing
Specimen Photography in Natural History Collections
C. M. KAI SER, H. KAISER, K. J. RICK ERL, M. O’SHEA ....................................... 666
Efficacy of Visible Implant Elastomer (VIE) Tag Retention in the Green
Anole, Anolis carolinensis, by Using ImageJ Color Analysis
S. D. UNGER, D. M. KEENAN .......................................................................... 677
AMPHIBIAN AND REPTILE DISEASES
Host and Geographic Range of Snake Fungal Disease in Tennessee, USA
M. GRISNIK, J. E. LE YS, D. BRYAN, R. H. HAR DMAN, D. L. MILLER,
V. A. COBB, C. OGLE, C. SIMPSON, J. R. CAM PBELL, R. D. APPLEGATE,
M. C. ALLE NDER, E. J. NORDB ERG, A. A. HOEKS TRA, D. M. WALKER ............... 682
A Preliminary Assessment of the Skin-Associated Microbiome of
Caecilia buckleyi (Amphibia: Caeciliidae)
K. L. KRYNAK, D. G. WESSEL S, E. B. SNYDER, T. J. KRYNAK, S. IMBA,
J. A. LYONS, A. H. LOUDON, J. M. GUAYASAMI N ............................................ 690
Earliest Record of Batrachochytrium dendrobatidis in Amphibian
Populations of Baja California, Mexico
G. S. BARR ERA, A. P. G ARCÍA ........................................................................ 693
CONSERVATION
Perspectives in Conservation ..................................................................701
GEOGRAPHIC DISTRIBUTION
Distributional Records of Amphibians and Reptiles from the Lower
James River Valley, South Dakota, USA
D. R. DAVIS .................................................................................................. 720
GEOGRAPHIC DISTRIBUTION............................................................................ 705
NATURAL HISTORY NOTES ................................................................................ 722
BOOK REVIEWS ...........................................................................................766
ZOO VIEW........................................................................................................... 774
INSTITUTIONAL PROFILE .................................................................................. 779
ART IN HERPETOLOGY ...................................................................................... 782
ABOUT OUR COVER ........................................................................................... 784
SSAR BUSINESS ................................................................................................. 784
NEWSNOTES ...................................................................................................... 807
MEETINGS .......................................................................................................... 809
OBITUARIES ....................................................................................................... 809
CURRENT RESEARCH ......................................................................................... 813